It is important for us to be able to understand the behaviour of primates in zoos for at least three
reasons: firstly as a means towards ensuring their welfare, secondly to use that understanding to
ensure a positive zoo experience for zoo visitors, and thirdly so that results of basic research
undertaken on zoo primates can be properly evaluated. Often, however, the results of studies of how
the zoo environment affects primate behaviour are not easy to interpret. We should recognize that the
zoo environment is only one of a number of environments in which primates live, and should identify
in which ways the zoo environment is different from those other environments. Here, it is suggested
that the zoo environment may be defined in terms of three dimensions: regular presence of large
numbers of unfamiliar humans, restricted space, and being managed. Individually all three of these
can also be found in other, non-zoo environments, but all three together are characteristic of zoo
environments. This paper is an initial attempt to compare studies of primate responses to the variables
associated with each of these three dimensions across different primate environments. It is concluded
that there is a need for at least two different types of study in future: comparisons across a range of
primate environments using the same species and measures, and studies of the interactions between
the three dimensions identified for zoo environments.
# 2004 Elsevier B.V. All rights reserved.

We now know quite a lot about the behaviour of captive primates. The last 20 or so years
have seen a great growth in the number of behavioural studies undertaken in zoos; some of
this is basic research designed to test theories from ethology and behavioural ecology, but
most of it is more applied and designed to tell us something about how captive
environments influence behaviour (Hosey, 1997). However, interpreting the results of these
studies, particularly those on the influence of the captive environment, can be difficult, for a
number of reasons, which are explored below.
One of the difficulties is that it is by no means clear what our benchmark should be for
evaluating the behaviours we see in captivity. Early attempts to increase the activity, and
decrease the abnormal behaviours, of captive animals, notably by Markowitz (Markowitz
et al., 1978; Markowitz and Stevens, 1978; Markowitz and Spinelli, 1986) often involved
presenting the animals with operant tasks for a food reward, a process generally referred to
as ‘‘behavioural engineering’’. This approach was open to criticism that, amongst other
things, it did not encourage natural behaviours (Hutchins et al., 1978a,b, 1984), and instead
an approach was advocated based on making cage structures and furnishings more
‘‘naturalistic’’ in order to promote naturalistic behaviours (Hancocks, 1980; Forthman
Quick, 1984; Maple and Finlay, 1989). Clearly, the maintenance of a naturalistic profile of
behaviour by captive animals was an important goal (McGrew, 1981; Tilson, 1986),
especially if captive-bred animals were ultimately to be released into the wild (Van Hooff,
1986; Redshaw and Mallinson, 1991a,b). However, an associated assumption, that the
behaviour of their wild-living counterparts should be a yardstick for us to assess the well-
being of captive animals, has been questioned (Veasey et al., 1996) on the grounds, among
others, that non-performance by captive animals of some of the behaviours shown by wild-
living animals does not necessarily indicate reduced welfare. Thus, evaluations based on
the welfare of the animals should be used in conjunction with wild-captive comparisons if
evaluation of well-being is our goal.
This potentially leads us to a further difficulty, which is about separating out the possible
effects of different environments. The problem of defining exactly what ‘‘wild’’ means for
primates was noted by Bernstein in the first ever International Primatological Society
Congress (Bernstein, 1967), and the continuing impact of human activity on primate
habitats has probably meant that many of the habitats where studies of wild primates are
currently carried out are not really equivalent to each other in terms of the way the animals
behave within those environments. At the other end of the wild-captive continuum, we find
a common assumption that primates kept in laboratories or primate centres show responses
to the captive environment which are equivalent to those shown by primates in zoos. This
assumption has not been tested. Somewhere within this wild-captive continuum we also
have to accommodate a variety of conditions variously referred to as ‘‘feral’’, ‘‘free-range’’
or ‘‘semi-free range’’, and which might include rhesus monkeys on Cayo Santiago
(Zorpette, 1995), lion-tailed macaques on St. Catherine’s Island (Fitch-Snyder, 1993), and
lemurs in large wooded enclosures at the Duke University Primate Centre (Simons, 1986).
The point has often been made that primates show great flexibility and adaptability (see,
for example, Lee, 1991) and that zoo environments for them should be somewhere within
their range of adaptability (Poole, 1991). However, separating out the effects of the zoo

At their most
extreme. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 109
environment. it is not captive
environments per se which cause the behaviour. Lukas.. interpreting
observations and experimental results remains difficult (Mason and Mendl.1. Fraser et
al.. 1984). of course.
2. Appleby and Sande. autoaggression (self-mutilation) can be a significant problem
in laboratory-housed primates (Chamove et al. we must identify the
particular variables involved and make comparison with a range of other situations. G. 2002). 1994. of paramount importance to zoos.
What does this mean for zoo primates? It is generally assumed that the zoo environment
is a more extreme one than the other environments in which primates live (with the likely
exception of laboratories). but is necessary if we are to establish any kind of theoretical framework in
which to evaluate the results of our studies on the zoo environment. Fraser and Duncan. Wiepkema and Koolhaas. in preparation). affects primate behaviour. and it
seems reasonable that welfare should be assessed in terms of what individual species have
evolved to be able to cope with (Barnard and Hurst. has not been attempted in any
systematic way. 1996). the effects of maternal
deprivation in human-reared chimpanzees can be ameliorated to some extent by bringing
the animals into a social group in a zoo environment (Martin. of
course. 1993. For example. Similarly. Nevertheless.
there is growing awareness that human impact on animal environments and habitats is not
just a conservation concern but also a welfare concern (Kirkwood et al. and for
us to be able to interpret that knowledge within a theoretical framework. This perspective recognizes that
wild-living animals face stressors too. and comparing them with the effects of the other environments that free-
living and captive primates might find themselves in. and in any case we need to
know in which particular aspects or variables the zoo environment is extreme.R. 1999) and stereotyped body rocking in chimpanzees (Pazol and
Bloomsmith. but in zoo primates does not seem to
occur very frequently (Hosey and Skyner. 1995). But for at least some abnormal behaviours. 1993). 1997. So to be able to
understand how zoo environments affect captive primate welfare. 1998. 1985. Broom and Johnson. 1993). is to understand better how variables
in the zoo environment can be manipulated to improve the welfare of captive primates. 1993. such as regurgitation and re-ingestion in gorillas (Akers and
Schildkraut. This paper is a first
attempt at making such a comparison. captive environments can cause abnormal behaviours that are rarely if ever seen in
wild environments. Sainsbury et
al. Animal welfare
Maintaining the psychological as well as the physical well-being of their animals is. Considerable advances have been made in
creating a theoretical and practical framework for understanding well-being and evaluating
animal welfare (e. Why this question is important
There are at least three reasons why it is important for us to know exactly how the zoo
environment. and can experience compromised welfare. but particular aspects of particular captive
environments.
...
2. 2002).g. this assumption needs to be tested. Indeed.
The other side of this particular coin. as opposed to other primate environments.

Kreger and Mench. 1995. notably Apenheul (Mager and Griede. by making it more likely
that zoo visitors will see active animals doing natural behaviours in an appropriate habitat. Dickie. on the one hand breeding rare species with a view to
eventual re-introduction to the wild.. 1995. For example. 2000). Live
demonstrations do have educational benefits (Heinrich and Birney. as managed
captive breeding can lead to production of surplus or non-breeding animals (Glatston. Objects
may be given to zoo primates for similar reasons (e.R. but much enrichment for zoo primates is intended to increase their foraging
time and associated behaviours (e. promotion of a behavioural profile similar to that seen in the wild is
often identified as the aim of the enrichment (e.g. awareness-raising and attitude changing
are also important. This. 2000). 2000).. Therefore. Britt. Vick et
al. Melfi and Feistner (2002) found that
activity budgets of Sulawesi macaques Macaca nigra were different in different zoos. Reinhardt and Roberts. ideally including
close contact with animals (Kidd et al. 2000). 1999) to describe them. and. 2000). 1998. 1986) and
Vallee des Singes (Vermeer. the aim of
enrichment is often to increase the activity of the animals and decrease their abnormal
behaviours.
Providing naturalistic. as the perceptions many people have of zoos are often negative (Finlay
et al. 1988. however. 1994).
. Swanagan.. 2000). identify conservation and education as their
priorities. in their mission statements. and in this respect the animals act as ‘‘ambassadors’’
furthering the conservation cause (Vermeer.
2. These
goals are much wider than just. and a range of techniques is used which varies from manipulation of the social
group to the provision of toys (Kessel and Brent. 2000). 1990. and should be tested for
each species. The zoo visitor experience
Most zoos. for
example. 1988. 1992).
Allowing close contact and even interaction between zoo visitors and free-ranging
primates is now a feature of several zoos.g. 1998) can play a large part in this process. Reade and Waran. Zoo visitor attitudes can become more
positive and people’s interest in the animals increased when they encounter free-ranging
primates (Price et al. 1998.g. For laboratory primates. and on the other hand providing the public with
information about exotic species. Rooney and Sleeman.2. Shepherdson. certainly in Europe and North America. should ideally be done within a framework which recognizes the
behavioural adaptability of many primates and the variety of wild and captive
environments in which they live. Renner
et al. actively pursue those goals. 1998). Howell and Fritz. and on a smaller scale has been introduced in otherwise
conventional zoos like Blackpool (Webster. Primates have also been used as living
demonstrations (Povada. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
There is now an enormous literature on environmental enrichment for primates (see... well-designed cages (Coe. 1994. 1985) and suitable environmental
enrichment (Robinson. For both goals. 1999. Lambeth and Bloomsmith.110 G. the assumption that zoos
represent an extreme environment for primates may not be correct. Here again. 1997. but
were not significantly different from the wild. Attitudes to conservation and awareness of the lives
of animals can be improved when people have a positive zoo experience. 1996). and those that promote live animal presentations in zoos
also use the term ‘‘ambassadors’’ (Gates and Ellis.
1998). Reinhardt. 2002). Mixing animals
and people need not conflict with the need to maintain for future re-introduction viable
naturalistic populations with behavioural profiles like those seen in the wild.

Some
primate research centres. de Waal and Van Hooff. long-term studies of chimpanzees at Arnhem (de Waal. we need to distinguish the zoo environment from other
environments in which primates live. comparison with a range of
other primate habitats will help us to evaluate the behaviour of primates used by zoos as
ambassadors. 1985).
1982. For example. Testing the assumption can show. have many superficial similarities to zoos.
3. 2002) and orangutans (O’Malley and
McGrew.3. and fruit smearing by chimpanzees (Fernandez-Carriba
and Loeches.. Again. Preuschoft et al. Scucchi et al. probably likely. for example.. 1993) have been
instrumental in refining our knowledge of group dynamics. as with the Sulawesi macaques
studied by Melfi and Feistner (2002). 2000). Defining the zoo environment
The first step in comparing primate responses to the zoo environment with their
responses to other environments is to identify exactly what are the independent variables
associated with the zoo environment. 1982. 2002). 1988. Behavioural research
Despite the popular myth that worthwhile behavioural research is not possible in zoos
because they are such an artificial environment.. Glander et al. that primate behaviour
is affected not by any single variable. It is possible. post-conflict behaviour. but much of it has made important
contributions towards developing and testing theory in behavioural biology. Schino et al. that zoo groups may not differ from wild ones in their
overall activity budgets.. For this reason. 1981. This is not as easy as it might at first seem.
Undoubtedly. and provided that their welfare is not compromised. 1985.
2. and Japanese macaques
at Rome Zoo (D’Amato et al. unusual behaviours such as tool
use by gorillas (Nakamichi. in reality not only is a substantial amount
of good research undertaken on zoo-housed animals. predation by woolly monkeys (Stearns et al. G. but by a number of zoo-related independent variables
acting together. it is perhaps less necessary that
these animals maintain a wild-type profile of behaviour. 1998). Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 111
1998). 1988) and lemurs (Jolly and
Oliver. 2001) may represent behaviours which also occur but are rarely seen in the
wild. and perhaps allow zoos to provide an experience which is enriching for both
the human and non-human primates. there may be other ways in which zoo groups do
differ from wild ones. bonobos (Gold. 1978.
That such effects on behaviour can contaminate behavioural studies is just an assumption. I propose the following three dimensions to
define the zoo environment and distinguish it from other primate environments:
. but might
differ from them in some important variables.R.
and needs to be tested. the results of behavioural studies on zoo primates must be interpreted in
the context of the possibility that the zoo environment has affected the animals’ behaviour. An advantage
of zoo primates is that the observer can detect subtle behaviours which may well be missed
in the wild. Nevertheless. Similarly...
alliances and coalition formation in primates. and it is important to compare zoos with a range of other primate
habitats so that these differences can be evaluated within an appropriate framework. 1984.

(1990. we can now look more closely at some of the
variables associated with each one in comparison with non-zoo primate environments. 1991a. Furthermore. If the
presence of those visitors causes an animal to retreat. Chamove et al. implying that the animals
viewed humans as agonistic competitors. then. By this. where the animals are routinely exposed only to humans
who are more-or-less known to them. Restricted space. Presence of zoo visitors
In order to achieve their mission objectives and also to be financially viable. the animals increased their locomotory activity and audience-directed
behaviours when active audiences were present (active audiences being those where at
least one person attempted to interact with or draw the animals’ attention).
3. Birke. then there is a very clear problem. were extensively thrown food by members of the public. become
stressed. but affiliative
behaviours were largely unchanged. similarly Cook and
Hosey (1995) found that chimpanzees were willing to enter into fairly long interaction
. 2002).. Thus. I mean the frequent (usually daily)
arrival of large numbers of people who are unfamiliar to the animals. it was generally found that agonistic
behaviours increased and affiliative (e. and groups of unknown visitors are rare. but were not
significantly affected by passive audiences (Hosey and Druck.R. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
1. across a range of primate species housed in
traditional cages. spatial accommodation. Group membership.112 G. Perret et al. which showed no visitor-related increase in
agonism.
Research of the past 20 or so years has not given a completely consistent picture of what
effect zoo visitors have on captive primates. 1988. become hidden or immobile. but in general the results of most studies can be
interpreted that most zoo primates find the presence of large active groups of visitors to be
stressful (Hosey.. The chronic presence of human visitors. 2000)..
1992c). If intra-group interactions were examined. A detailed series of studies undertaken by Mitchell et al. However. healthy animals.
the green monkeys in Fa’s (1989) study. zoos must
not only admit the public but must also give them an enjoyable and positive experience
based upon seeing and perhaps even interacting with active. 1984.. 1992a.
Having identified these three dimensions. 1987. 1995. for example. the male and female monkeys directed
their aggression to different targets among the human audience. feeding routine. The physical space available to even the most naturalistic groups of
zoo primates is usually much less than they would range over in the wild. Most aspects of the life histories of zoo primates are managed to some
extent by humans. However. Lukas et al.
2. Mitchell et al. health
and reproduction are all largely outside the animals’ control. such changes have not been seen in all studies
(Fa. 1989. would
exclude most primate centres.
Wormell et al.
It was suggested long ago by Morris (1964) that visitors might provide zoo animals with
welcome variability in an otherwise monotonous existence. Being managed.g..
4. grooming) behaviours might increase or decrease
under audience conditions (Glatston et al.. 1996. or start to show abnormal behaviours. but the possibility that
audiences might be enriching for some zoo primates has not really been tested. This.b) on golden-bellied mangabeys showed that the animals increased
visitor-directed and within-group aggression when audiences were present.b. 2002).

and must try to identify what particular variables of the human audience
cause which. and indeed with those allowed to free-range in the zoo. the rhesus macaques Macaca mulatta scrounge and beg for food. 1992). when the only apparent reward was an occasional
piece of food being thrown. Bali and India would seem to be that close proximity between human and
non-human primates need not be stressful for either.. G. Small (1998) compared long-tailed
macaques Macaca fascicularis at three different tourist temples in Bali.000/ha/year and are routinely fed by visitors
as well as being provisioned by the army (Fa. Fa (1992) reports that people-directed aggression is
very low in semi-natural macaque enclosures elsewhere in Europe. gorillas appear to habituate more
readily than chimpanzees to the presence of human observers in wild populations when
provisioning is not used (Tutin and Fernandez.
1987. unless properly managed. but levels of visitor-directed
aggression are high.
Tutin and Fernandez (1991) found that gorillas responded to sudden human presence
mostly with curiosity. (2003) found virtually the opposite response
pattern for the two species. The meagre data from wild primates
. Few
studies have collected systematic data on the responses of these animals to human visitors. if any responses. they were
particularly aggressive at a temple where ‘‘tourist guides’’ acted aggressively towards
them. could influence this. and chimpanzees mostly with flight. and
are generally tolerated by the human population (Southwick and Siddiqi. 2002). On Gibraltar. of resulting in increased intra-
group and visitor-directed aggression. and warns of the possibility of this as well as visitor-directed aggression in zoo
primates (Fa. he also points out that
feeding by the public has had an adverse effect on the reproduction of the Gibraltar
macaques. 1989). A later study by Werdenich et al. they interpreted the animals as
perceiving humans initially as unfamiliar species rather than as potential predators or
competitors. both in terms of chronic large
crowds and in terms of occasional short exposure. Subsequent encounters with humans could be negative or neutral. we might expect from casual observation that the animals would find the presence of
people less stressful. In general. In comparison. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 113
sequences with members of the public. but pointed out that other variables. 1991. such as the activity of the
observers. is by no means a condition that only zoo
primates experience. Mitchell et al. The lesson
from Gibraltar. but that the introduction of feeding by
the audience has the potential. 1992a) and noisiness (Birke.
Other places where non-captive primates are exposed to large numbers of human
visitors include some temples in Asia.
Non-captive primates who do not live in proximity to human settlements may also
receive regular human visitors. and found
differences between them in the amount of aggression they showed to humans. In Indian cities. Data so far implicate audience activity (Hosey and Druck. not to mention possible long-term reduction of the
animals’ fertility and impairment of health. 1991).R. For example.
We should also note that exposure to a human audience.
There is a clear need for more audience studies to be undertaken with primates in more
modern naturalistic cages. but not in the numbers seen at zoos and tourist sites. but were
not positive. in both
cases. however. There are few data on changes in
the animals’ behaviour when the public are present. 1998). 1992). non-captive barbary macaques Macaca sylvanus are
exposed at one site to visitor densities of 238. We must also recognise that audience presence is a condition rather
than a variable. mostly as a consequence of people being bitten by monkeys they have
provoked (Fa.

do not daily encounter large groups of
unfamiliar humans.R. non-zoo conditions. 1988).
Unfortunately. (1987) found that intra-group and visitor-directed aggression were high among the
chimpanzees at a research centre in Texas on days when visiting scientists and students
were touring the centre. along with the results from physiological studies (Clarke et al.
. three times as many episodes of wounding among the chimpanzees in periods
(weekdays) when human activity was greatest.
1997). though we should at the moment regard these as no more than working
hypotheses. so we should
not expect a uniform response pattern to human audiences across all the different primate
species that are kept in zoos. 1988). tourist areas) to those they do
not. like those in zoos. aggressive (rhesus macaques) or affiliative (bonnet macaques).
From all of these studies... three different
macaque species were subjected to the passive presence of a single human observer. What this tells
us is that different species are likely to respond to a stressor in different ways. unfortunately.
(c) Both captive and non-captive primates appear to habituate to humans they encounter
regularly. so a comparison between zoos and research centres would be an ideal
way of looking at the extent to which captive primates do habituate to their audiences. In one study (Clarke and Mason.114 G. The extent of this habituation may also depend as much on species-typical
response patterns as on the amount of exposure to humans. some wild-living primates live in close proximity to humans and
may encounter and interact with them regularly.
on average. Thus. Data from these studies do not permit direct comparison with
zoo chimpanzees. there is less opportunity than in zoos for the animals to habituate
to unfamiliar visitors. compared to weekends (Lambeth et al. with a
number of different behavioural measures being taken. however. unlike zoos. and that these can be reduced by changing the design of
the cage (Rumbaugh. The results. 1995. though there are some data from
chimpanzee colonies which suggest that zoo animals do habituate to some extent.
Primates housed in research facilities. we can make some tentative conclusions about audience
presence. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
do not. 1998) such high
levels of aggression have not been seen. allow us to make any worthwhile comparisons which would give us
insights into the habituation of zoo primates to their human visitors. The animals. Often food appears to be the
motivation for contact in these situations. Maki et
al. Wood.. are exposed to chronic human
contact from familiar humans. and perhaps also in some situations (e. a small number of studies on responses of primates to humans in
captive. Others have observed that laboratory chimpanzees show vigorous aggressive
displays to unfamiliar intruders.
There are. perhaps reflecting different social organisations and different typical species
responses to environmental events. but. Clearly more studies are needed to test these and establish them more firmly:
(a) Different species of wild-living primates probably respond to humans in different
ways. but in those studies where zoo chimpanzee responses to human visitors
have been examined (Cook and Hosey.
1988) allowed the three species to be characterised as reactive and fearful (crab-eating
macaques). normally housed in
groups in outdoor enclosures were housed in individual cages in a primate room for the
experiment. Subsequent analysis of laboratory records showed that there were.
(b) In some situations. such a comparison has yet to be made. 1995. Perret et al.g. zoos.

A series of experiments on pig-
tailed macaques (summarised in Erwin. Early studies considered that crowding.g. but in a restricted area
where presumably the public were not allowed access. and it did indeed result in
increased aggression.
What about primates in zoos? Waterhouse and Waterhouse (1971) studied the rhesus
macaque group in the Monkey Temple at Bristol Zoo. Here again. Finlay et al.) to give the animals more control over their encounters
with humans is likely to make the whole process of habituating to. will have different
responses to restricted space in captivity. and found a mean of 4. one of the most negatively perceived features of the zoo environment
is the restricted space afforded to the animals. 2000). a perception often expressed in terms of the
confinement of the animals and their inability to roam as they do in the wild (Rhoads and
Goldsworthy. it is also
likely that different species.
As with audiences.
we must recognise that captive and non-captive primates can live in a variety of situations
and that not all of them afford the animals unrestricted space.
5. etc. indeed the animals showed more
aggression when two rooms were available than only one.. Space reduction was only one of
Southwick’s manipulations with his rhesus monkey group. though currently
there are no direct data to support this suggestion. Novelty is an important
confounding variable and is often more responsible for behavioural change than changes in
the physical size of the cage (Nash and Chilton. For example. so to that
extent the animals are still constrained by boundaries of some sort. a
comparison of different primate environments shows that the effects of physical space are
more complex than this suggests. 1979. 1999. 1988). 1986) at a primate centre also failed to find a
simple connection between aggression and space. social variables seemed
to interact with the spatial variables. during that time the troops have maintained virtually the same
home ranges and core areas (Jolly and Pride. with different ranging patterns in the wild. interacting with.4 fights per
. However.
would result in elevated levels of aggression. allowing free range. but suggested
that the most severe aggression was related more to the change of being put into an
unfamiliar enclosure than to the space reduction per se. However. A similar
experiment by Alexander and Roth (1971) on Japanese macaques housed at a primate
centre also showed increased levels of aggression when space was reduced. G. and interpretation of studies can be difficult. However. ring-tailed
lemurs Lemur catta have now been studied at the Berenty Reserve in southern Madagascar
for some 40 years. 1986). there are a number of variables associated with the space that
primates occupy. through naturalistic
enclosures. and
coping with humans a much easier and less stressful one for the animals. Again.R.
although at least one (Southwick. Restricted space
For many people. Most of these studies were laboratory-based. as appears to be the case in carnivores (Clubb and
Mason. his overall conclusion was that social changes had a much
greater impact on levels of intra-group aggression than environmental changes. 1979. 2003). as with the presence of human visitors. Mertl-Milhollen. Again. 1967) was undertaken in a zoo. which could be achieved
experimentally by reducing the physical space or by increasing the number of animals. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 115
We can perhaps add that altering the conditions of captivity (e.

.. Surprisingly. for
example. Chimpanzees in laboratory cages.5 fights per hour when half the animals had
been removed. then increasing the complexity of
their enclosures should have measurable effects on their behaviour consistent with both
improved welfare and a more naturalistic profile of behaviour. and sometimes the results can be surprising.
If cage complexity is so important to captive primates. Nevertheless. Wilson (1982).
The physical dimension of the space is not the only variable associated with space that
has any significance for primates.b).
Stoinski et al. such as trees and rocks.b). when transported in pairs in
small cages. for instance.R. Even in laboratory cages. Gorillas. and
they used other social behaviours to maintain amicable social relationships when
threatened by crowding-induced stress (Nieuwenhuijsen and de Waal. 1994). They considered that fighting was a social pathology in response to over-
crowding. in both these studies
the gorillas showed strong preferences for areas near structures.. each had a preferred site where
they spend most time (Bettinger et al.
Among four female chimpanzees on a zoo island exhibit. 1985). often prefer to spend time close to their holding buildings (Ogden et al. extensive study of the chimpanzees in the naturalistic enclosure at
Arnhem showed that aggression rose only slightly when the animals were crowded. 2000). She concluded that providing large enclosures which contained a lot of movable
objects and provided social opportunities for the animals promoted higher levels of activity
in the orangutans. 1982). measured the activity of
animals in 43 groups of gorillas and 68 groups of orangutans in 41 different zoos. 2001a. usable area or feeding frequency. 2001a.
few studies have tried to identify exactly how much use animals make of the space or
structures in their enclosures. consolation. typically sat facing away from each other. We now
know much more about the behaviours many primates use to avoid the damaging effects of
aggression (e. For example. 1994) and may also prefer perimeter areas and even smaller cages
(Traylor-Holzer and Fritz. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
hour when 41 animals were present. which usually have
less space and structural complexity than zoo enclosures. in a naturalistic enclosure with high
moulded trees and vines but a flooded floor. 1989. The best
predictors of activity in the groups were number of animals and the presence of objects
rather than enclosure size. but only 1.g.
Complexity of space is usually increased by the provision of structures.
Other observations also imply that primates cope behaviourally with crowding. avoidance) and can see that these allow captive
groups to live relatively peacefully in restricted space (de Waal.. However. de Waal et al.. prefer levels above the
cage floor (Goff et al. for example. A further study by Perkins
(1992) looked only at orangutans and used multiple regression to identify important
variables. This can result in spatial use of the enclosure very similar to the use
of space seen by animals in the wild. for
example Kummer (1982) mentioned that hamadryas baboons.. 1993. with the
naturalistic environment being the clearest attempt to provide structural complexity similar
to that seen in the wild. 2000). which might be interpreted as a
conflict avoidance strategy. Several studies have shown that the complexity of the
space is more important than its size.116 G. orangutans spent most time sitting and
reclining in the upper canopy and avoided the floor (Hebert and Bard. reconciliation. and in one zoo have been estimated to spend 50% of their time in
less than 15% of the exhibit (Stoinski et al. A very large literature
suggests that this is the case. animals’ use of cage space is
often not uniform. with complexity being increased by structural changes to cage
.

1986.
McKenzie et al. 1986.R. in fact the activity patterns in both kinds of housing were within the range of
variation seen in the wild. 1999) and by releasing animals into free-range (Price et
al. 1991. Thus. 1982. O’Neill et al. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 117
furnishings and substrates (e.g. Examples of
management of these populations include provisioning of macaques for tourist and
research purposes (e. capture of animals for
marking and measurement (e. at
least in terms of the behaviour of the animals that occupy them...g. Ludes-Fraulob
and Anderson.
What these and other similar studies tell us is that restricted space per se need not be a
welfare problem and need not lead either to the loss of species-typical behaviours or the
acquisition of abnormal behaviours provided that the components of the space (particularly
structural complexity) are appropriate and give behavioural opportunities.. Similarly Little and Sommer (2002). the Sulawesi
macaque groups studied in zoos by Melfi and Feistner (2002) did not differ significantly in
their activity budgets from animals in the wild. Chamove and Rohrhuber. It
should.. 1992.
For many people. 1999) and maintenance of free-living or provisioned populations in areas
where they may or may not be native (e. we may
question. Jensvold
et al. 1992.g. and low foraging and feeding
times are often found in their activity budgets compared to those in the wild (e. Britt. Peignot et al. Price. O’Leary. Bayne et al.
since some behavioural change is not reflected in activity budgets. Zucker et al. Clarke et
al. 1996. the most obvious way in which zoo and laboratory primates lead
different lives from their wild counterparts is in the fact that they are supplied with regular
food. or of tourist interest. McGrew et al.
over a variety of captive and non-captive environments. however.g.
. be remembered that many populations of primates that are regarded as
wild or free-range are also managed to some extent. 1993). Hill. 1991. Goerke et al. Traditionally food has been
presented to captive primates in a ready-processed form. Being managed. of course..
Ogden et al. Certainly. is also a
significant feature of the lives of laboratory primates. Fa. 1987. More direct wild-captive comparisons of this sort are needed...g. G... 1987. and using additional measures. by moving animals into more naturalistic enclosures (e.
1999). Anderson and Chamove. 1999). whether
the best zoo enclosures are particularly different at all from non-captive environments. 1992.g. 2001). because they are pests. and it is likely that the impact of
management on their behaviour is somewhat different from that of zoo primates because
of the differences in the other two dimensions. Garrison and White. Altmann. or of research interest. Macedonia. found that while there were behavioural
changes. Brent.. who
studied a group of Hanuman langurs Presbytis entellus in a traditional cage and again after
a move to a new style naturalistic enclosure. 1989. and therefore do not need to spend time finding food. 1990. 1962) and veterinary procedures (Laudensla-
ger et al. 1999). 1991....
6. 1999. 1984. Chang et al. and
this can have considerable impact on their behaviour. Being managed
Most aspects of the lives of zoo primates are managed to some extent by humans. in terms of restricted space being a dimension of the zoo environment. by moving animals from indoor to outdoor enclosures (e.g. or of
conservation importance. 1989. presence of public and amount of space. Dierenfeld and McCann.

2003). For example.
where the regular alternation of enclosures may simulate. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
1998). In laboratory conditions. Catherine’s Island eat a variety of native
plants that they would not encounter in their original environments (Dierenfeld and
McCann. 2001). which involved orangutans and siamangs as well as tapirs. animals may. 1994). and the effects and welfare implications of this have hardly
been studied. 1983) and chimpanzees (Howell et al.
. The effects of changes to cage furnishings or design. may benefit from brief threatening events. This can
involve different groups of the same species.
which may have consequences for their behaviour. 1993). for example gorillas (Lukas et al. Here again.118 G. 2003). 1999). Another behavioural
change in captive primates related to feeding is pre-feeding agonism. for example they may
show increased affiliation and new behaviour patterns when confronted with occasional
stimuli such as a model bird flying overhead (Moodie and Chamove. 2001). which again may have behavioural consequences. for example in
baboons (Wasserman and Cruikshank. however. several studies have advocated regular moving
of animals between enclosures as a way of increasing activity and enclosure use.. Zoo primates may also be exposed to foods that are not
a part of their normal natural diet (Nijboer and Dierenfeld. tigers and babirusa. we
do not have sufficient data to know if zoo and laboratory primates are affected in different
ways by such stimuli. be exposed to scents of
their predators or their prey. As with the other
variables we have considered. resulting in animals that are heavier than their wild counterparts (Schwitzer and
Kaumanns. or different species may be rotated. 1999). diets in captivity may lead to
obesity.. is through changes to cages. Campbell et al. and ring-tailed lemurs
and lion-tailed macaques living free-range on St. and may therefore show behavioural
change. or moves to new enclosures...
1984) and providing opportunities that the animals get in the wild (McGrew et al. 1986).
are most studied when they involve enrichment or a move from a traditional to a naturalistic
enclosure (see previous section). scattering food in the substrate (Anderson and Chamove. provisioned groups of Japanese macaques show greater agonism and
differences in other social behaviours compared to unprovisioned groups (Hill. 1990). 1995) and positive reinforcement training
(Bloomsmith et al. as in the study by White et
al.
Another way in which zoo primates are managed. (2003). Thus. 1993). these aspects of feeding management can also be found in
non-captive primates. for example by supplying whole rather than
chopped fruit (Smith et al.
Attempts to manage pre-feeding agonism include the use of unpredictable feeding
schedules (Bloomsmith and Lambeth. vervet monkeys living in Entebbe who have access to
human food show more time resting and less time feeding than their ‘‘wild’’ counterparts
(Saj et al..
can significantly change behaviour in a more naturalistic direction. Finally..R. ranging
behaviours seen in the wild. Recently. among other things.. changes to group composition. cotton-top tamarins Saguinus oedipus show
elevated anxiety responses to faecal scents of predators compared to scents of non-
predators. It has. Changing the way food is presented. and the animals were affected by whoever had
previously been in the enclosure.
More species-typical behaviours were seen. and proximity to other
species. but
also show more innovative behaviours (Huffman and Hirata.. 1999). 1996. for example. 1989). which may have welfare implications for how these animals are housed in zoos
(Buchanan-Smith et al. though these techniques have generally been tried with
laboratory rather than zoo primates.
again in laboratories. also been suggested that captive tamarins.

tamarins attacking viscachas and agoutis. Infants may also be
introduced to potential foster parents as an alternative to hand rearing (Kerridge. 1988: squirrel monkeys).. G.
Often introductions of animals into groups occurs because the animal in question has
been hand reared and/or is asocial because of early social deprivation... 1996. Understanding and
evaluating the welfare and behaviour of hand reared... but also in species like ruffed lemurs (Romano
and Vermeer. 1998. is
not easy. a good knowledge of the
behavioural biology of the species in the wild is needed before undertaking social
manipulations (Visalberghi and Anderson. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 119
Zoo primates are. however. and have varying levels of success.
such as seasonal separation and subsequent re-integration of males and females (Williams
and Abee. 1995. and young
barbary macaques and barbary sheep playing together.. 1972. 1999:
ruffed lemurs). Captivity imposed changes can include merging of
groups (Araguete et al. pair or group housing has long been
advocated as a social enrichment and a number of studies have documented the behavioural
changes associated with a change in the social environment (Reinhardt et al.
Even in non-captive situations primates may be subjected to some of the management
practices described above. McCann and Rothman. How to interpret these responses in
terms of the welfare of the animals concerned. Such introductions are often accompanied by initial
aggression. 1990. 1987). Jendry. Burks et al. Brent et al. Pullen. often maintained in mixed species groups.. introducing new individuals into existing
groups (Scruton and Herbert. 2003) and lion-tailed macaques (Stahl et al.
1996. and sometimes these may reflect social processes that also occur in the wild.. 1988. In laboratories and primate centres.
Few studies have been undertaken on these groups. Hoff et al. Pfalzer and Ehert. let alone the naturalism of their behaviour. 1989. 1988) and ruffed lemurs (Brockman et al. Ryan et al.. siamangs (Parker et al. 1995).. which may be kept as bachelor groups.R. 1999) as perhaps being similar
to zoo lemurs being released into a naturalistic enclosure. Fritz. orangutans
(Hamburger. an owl monkey building up a relationship with a male sloth. fostered and single-sex grouped
animals may not be particularly helped by simple comparisons with the wild. 1997) and introducing individuals to each other prior to putting both into
an existing group (Meshik. 1988). 2002) but also for species as diverse as chimpanzees
(Pfeiffer and Koebner.
Changes to the composition of captive primate groups can also have profound effects on
behaviour. 1993). release of ruffed lemurs into
. 2000). There is quite a large
literature on this for gorillas (Meder.
But changes to group membership may be carried out both in laboratories and zoos for
other reasons. 2001b. 2001). A further consequence of the captive management of primate populations
can be surplus males. but may
benefit from comparisons across all the different captive and non-captive situations in
which primates live. but Ziegler (2002) surveyed mixed
species exhibits in German zoos and found that although in some of them the different
species appeared to ignore each other. 1986).. Seres et al. 1985. Clearly. 2001. 1999). Catherine’s Island (Keith-Lucas et al. sometimes other
primates but often non-primate species which they may or may not encounter in the wild. As representative examples. 1978.. 2001. Inglett et al. we can point to the release of ring-
tailed lemurs onto St. Japanese macaques riding on and
grooming barbary sheep.. notably in gorillas (Stoinski et
al. this symposium). baboons stealing eggs from ostriches. in others there were inter-species interactions which
included: baboons riding on and grooming elephants.
1999.

1997) as being rather like some of the movements of captive primates between
zoos.
Some of this similarity can be seen in Table 1. as do the categories ‘‘zoo’’.
However. in
some of these variables zoo and some wild environments are becoming more similar. Lee et al. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129
Madagascar (Britt et al... and many species have to change their ecology and behaviour in
order to survive (see. However. and how they may also occur in other primate
environments
Zoo Laboratory/research centre Wild
Humans
Regular unfamiliar audience Yes No Some
Regular familiar small number of people Yes Yes Some
Occasional unfamiliar people No Yes Yes
Space
Small. for example.. So. Even other non-captive groups. pests
or tourist features. Johns and Skorupa. if any. or because they raid human crops and garbage (e. Else. restricted space and being managed are crucial to
furthering our understanding of this environment. how
the combined effects of all of these different practices lead to differences.
But it would be a mistake to assume that wild environments are characterised by a lack
of these features. Forthman Quick. Clearly. Johns. 1991). may be regularly provisioned with food by people (Hill. it seems at least pragmatically clear that
the three factors of audience presence.
As can be seen. between
different captive and non-captive groups of primates. Human impact means that the space available to non-captive primates is
declining all the time.g. 2004) as an example of integrating animals into existing groups.g. 1986.120 G. Many non-
captive primates already regularly encounter humans through tourism (e.R. 1987. 1999). that are not hunted.
1986).
and proposals for translocating rhesus and hanuman monkeys for conservation purposes
(Pirta et al. the features identified there each
show considerable variability.
7. there is evidence available about the impact on behaviour of a number of
management procedures used on captive primates in zoos and laboratories.
1991) or because they are hunted. is currently unclear. Discussion
As we can see from the above review. there are obviously difficulties in defining exactly
what the zoo environment consists of. ‘‘laboratory’’ and ‘‘wild’’. it would be simplistic to infer from this that the zoo environment can be
Table 1
Some of the variables that may affect zoo primate behaviour. However. not naturalistic Some Some No
Small naturalistic Some Some Some
Large naturalistic No No Some
Managed
Food supplied Yes Yes Some
Getting caught/handled Yes Yes Some
Getting moved around Yes Yes Some
Encountering other species Some Some Yes
.

5. Standards in Laboratory Animal
Management.. C.L.
99–109. 338–435. With systematic comparisons
across different environments.. there is also a clear need for research into the combined effects of visitor
presence. S. 73–90. To do this effectively.R. we need to
undertake more comprehensive comparisons of the behaviour of different species in a
range of captive and non-captive environments.
Anderson. Philosophical debate on the nature of well-being: implications for animal welfare. cage complexity and management processes on the behaviour of zoo primates. Hosey / Applied Animal Behaviour Science 90 (2005) 107–129 121
equivalent to the wild for captive primates.
We also need to look more closely at how the different variables associated with the zoo
environment interact with each other. Hurst. J.M. Reactions of adult and immature squirrel
monkeys to intergroup exposure... 4.
Araguete. 17. which helped greatly
improve the manuscript.J. 1996. 1998. Sci. Regurgitation/reingestion and coprophagy in captive gorillas.. M.. and more knowledge about the interactions between
variables. 1985. Mason.. D. Welf. N.. 1998) that they
do.S. J. UFAW. Potters Bar.
Appleby. 11.
Behaviour 39. 2002.
However.
.
102. Zoo Biol. 1971. Welfare by design: the natural selection of welfare criteria..Y. see Wood.
Anim. I would like to thank the two
anonymous referees for their encouraging and positive comments.
Altmann. Mendoza.
Barnard. Lyons. Macaca mulatta.
References
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Acknowledgments
My thanks to Vicky Melfi for all her help and support. The effects of acute crowding on aggressive behavior of Japanese monkeys. G.A. D.. So. S. Allowing captive primates to forage. as there is evidence (e. The goal of the modern zoo is to provide
environments which are within the range of behavioural adaptability for the animals.S. vol. Roth.g. Zoo Biol. by
definition.. Ann. P.
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it important to do the comparison. we will be a step closer to providing a much-needed theoretical framework
within which the behaviour of zoo primates can become more understandable. as it is
also clear that there can be great variability within the same species in the behaviour of
primates in different non-captive environments. 1984.
because the indications are that variability within different environments may be greater
than the variability between them. 1962..S. W. UK... 405–
433. even the limited comparison undertaken here gives some reason for optimism. 2. E. pp. J. 519–524. A field study of the socio-biology of rhesus monkeys.P. that research on zoo primates
may not necessarily be affected by systematic bias in comparison with studies done in the
wild.. Thus.